Basal Dendrites of Layer-III Pyramidal Neurons do not Scale with Changes in Cortical Magnification Factor in Macaque Primary Visual Cortex.

Tomofumi Oga,Ichiro Fujita,Tsuguhisa Okamoto

doi:10.3389/fncir.2016.00074

Abstract

Neurons in the mammalian primary visual cortex (V1) are systematically arranged across the cortical surface according to the location of their receptive fields (RFs), forming a visuotopic (or retinotopic) map. Within this map, the foveal visual field is represented by a large cortical surface area, with increasingly peripheral visual fields gradually occupying smaller cortical areas. Although cellular organization in the retina, such as the spatial distribution of ganglion cells, can partially account for the eccentricity-dependent differences in the size of cortical representation, whether morphological differences exist across V1 neurons representing different eccentricities is unclear. In particular, morphological differences in dendritic field diameter might contribute to the magnified representation of the central visual field. Here, we addressed this question by measuring the basal dendritic arbors of pyramidal neurons of layer-IIIC and adjoining layer III sublayers (in the Hassler’s nomenclature) in macaque V1. We labeled layer-III pyramidal neurons at various retinotopic positions in V1 by injecting lightly fixed brain tissue with intracellular dye, and then compared dendritic morphology across regions in the retinotopic map representing 0–20° of eccentricity. The dendritic field area, total dendritic length, number of principal dendrites, branching complexity, spine density and total number of spines were all consistent across different retinotopic regions of V1. These results indicate that dendrites in layer-III pyramidal neurons are relatively homogeneous according to these morphometric parameters irrespective of their locations in this portion of the retinotopic map. The homogeneity of dendritic morphology in these neurons suggests that the emphasis of central visual field representation is not attributable to changes in the basal dendritic arbors of pyramidal neurons in layer III, but is likely the result of successive processes earlier in the retino-geniculo-striate pathway.

Highlights

In the mammalian primary visual cortex (V1), visual information from the left and right visual fields is processed in the contralateral hemisphere
How much cortex is devoted to a given visual field can be quantified by the cortical magnification factor, which is defined as cortical surface area divided by the size of visual field represented in it
The dendritic morphology of layer-III pyramidal neurons was uniform across 0–20◦ representation in the retinotopic map of V1

Summary

Introduction

In the mammalian primary visual cortex (V1), visual information from the left and right visual fields is processed in the contralateral hemisphere. The retinotopic map was independently discovered by Inouye (1909); (translated in Glickstein and Fahle, 2000) and Holmes and Lister (1916) by analyzing the spatial relationship between visual field deficits and the gunshot path through the skull of wounded soldiers As these pioneering studies already noticed and later studies on human and animals detailed, the foveal visual field is represented by a large cortical surface area, while gradually smaller areas are allocated to more peripheral visual fields (Daniel and Whitteridge, 1961; Gattass et al, 1981, 1987; Tootell et al, 1982; Van Essen et al, 1984; Fritsches and Rosa, 1996). If the amount of divergent and convergent retinal projections to V1 is constant across visual eccentricities, the cortical magnification factor should decrease from center to periphery at the same rate as the RGC density Assuming this linear relationship, the cortical magnification factor in the squirrel monkey fovea (at 0.5◦) should be about 235 times larger than that in the periphery (at 50◦). Changes in cortical magnification factor roughly parallel those in RGC density, but full explanation needs further neuronal mechanism that amplifies the emphasis of the central visual field (Myerson et al, 1977; Schein and de Monasterio, 1987)

Methods

Results

Conclusion